Table of Contents
Cardiovascular Psychiatry and Neurology
Volume 2011, Article ID 469046, 10 pages
http://dx.doi.org/10.1155/2011/469046
Research Article

Effects of Neonatal Systemic Inflammation on Blood-Brain Barrier Permeability and Behaviour in Juvenile and Adult Rats

1Department of Pharmacology, University of Melbourne, Medical Building 181, Parkville VIC 3010, Australia
2Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford OX13QX, UK
3Institute of Stem Cell Research, Helmholtz Zentrum München, 85764 Neuherberg, Germany

Received 11 August 2010; Revised 9 January 2011; Accepted 18 January 2011

Academic Editor: Alon Friedman

Copyright © 2011 H. B. Stolp et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. S. Brown, “Prenatal infection as a risk factor for schizophrenia,” Schizophrenia Bulletin, vol. 32, no. 2, pp. 200–202, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. K. B. Nelson and R. E. Willoughby, “Infection, inflammation and the risk of cerebral palsy,” Current Opinion in Neurology, vol. 13, no. 2, pp. 133–139, 2000. View at Google Scholar · View at Scopus
  3. C. A. Pardo and C. G. Eberhart, “The neurobiology of autism,” Brain Pathology, vol. 17, no. 4, pp. 434–447, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. H. B. Stolp and K. M. Dziegielewska, “Review: role of developmental inflammation and blood-brain barrier dysfunction in neurodevelopmental and neurodegenerative diseases,” Neuropathology and Applied Neurobiology, vol. 35, no. 2, pp. 132–146, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. H. B. Stolp, K. M. Dziegielewska, C. J. Ek et al., “Breakdown of the blood-brain barrier to proteins in white matter of the developing brain following systemic inflammation,” Cell and Tissue Research, vol. 320, no. 3, pp. 369–378, 2005. View at Publisher · View at Google Scholar · View at Scopus
  6. T. Debillon, C. Gras-Leguen, S. Leroy, J. Caillon, J. C. Rozé, and P. Gressens, “Patterns of cerebral inflammatory response in a rabbit model of intrauterine infection-mediated brain lesion,” Developmental Brain Research, vol. 145, no. 1, pp. 39–48, 2003. View at Publisher · View at Google Scholar · View at Scopus
  7. F. H. Gilles, D. R. Averill, and C. S. Kerr, “Neonatal endotoxin encephalopathy,” Annals of Neurology, vol. 2, no. 1, pp. 49–56, 1977. View at Google Scholar · View at Scopus
  8. C. Mallard, A. K. Welin, D. Peebles, H. Hagberg, and I. Kjellmer, “White matter injury following systemic endotoxemia or asphyxia in the fetal sheep,” Neurochemical Research, vol. 28, no. 2, pp. 215–223, 2003. View at Publisher · View at Google Scholar · View at Scopus
  9. Y. Pang, Z. Cai, and P. G. Rhodes, “Disturbance of oligodendrocyte development, hypomyelination and white matter injury in the neonatal rat brain after intracerebral injection of lipopolysaccharide,” Developmental Brain Research, vol. 140, no. 2, pp. 205–214, 2003. View at Publisher · View at Google Scholar · View at Scopus
  10. C. I. Rousset, S. Chalon, S. Cantagrel et al., “Maternal exposure to LPS induces hypomyelination in the internal capsule and programmed cell death in the deep gray matter in newborn rats,” Pediatric Research, vol. 59, no. 3, pp. 428–433, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. H. B. Stolp, K. M. Dziegielewska, C. J. Ek, A. M. Potter, and N. R. Saunders, “Long-term changes in blood-brain barrier permeability and white matter following prolonged systemic inflammation in early development in the rat,” European Journal of Neuroscience, vol. 22, no. 11, pp. 2805–2816, 2005. View at Publisher · View at Google Scholar · View at Scopus
  12. X. Wang, G. Hellgren, C. Löfqvist et al., “White matter damage after chronic subclinical inflammation in newborn mice,” Journal of Child Neurology, vol. 24, no. 9, pp. 1171–1178, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. G. Loron, P. Olivier, H. See et al., “Ciprofloxacin prevents myelination delay in neonatal rats subjected to E. coli sepsis,” Annals of Neurology. In press.
  14. L. W. Fan, Y. Pang, S. Lin, P. G. Rhodes, and Z. Cai, “Minocycline attenuates lipopolysaccharide-induced white matter injury in the neonatal rat brain,” Neuroscience, vol. 133, no. 1, pp. 159–168, 2005. View at Publisher · View at Google Scholar · View at Scopus
  15. U. Meyer, M. Nyffeler, A. Engler et al., “The time of prenatal immune challenge determines the specificity of inflammation-mediated brain and behavioral pathology,” Journal of Neuroscience, vol. 26, no. 18, pp. 4752–4762, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. L. Shi, S. E. P. Smith, N. Malkova, D. Tse, Y. Su, and P. H. Patterson, “Activation of the maternal immune system alters cerebellar development in the offspring,” Brain, Behavior, and Immunity, vol. 23, no. 1, pp. 116–123, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. M. E. Fortier, G. N. Luheshi, and P. Boksa, “Effects of prenatal infection on prepulse inhibition in the rat depend on the nature of the infectious agent and the stage of pregnancy,” Behavioural Brain Research, vol. 181, no. 2, pp. 270–277, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. L. Shi, S. H. Fatemi, R. W. Sidwell, and P. H. Patterson, “Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring,” Journal of Neuroscience, vol. 23, no. 1, pp. 297–302, 2003. View at Google Scholar · View at Scopus
  19. Y. Pang, L. W. Fan, B. Zheng, Z. Cai, and P. G. Rhodes, “Role of interleukin-6 in lipopolysaccharide-induced brain injury and behavioral dysfunction in neonatal rats,” Neuroscience, vol. 141, no. 2, pp. 745–755, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. S. D. Bilbo, J. C. Biedenkapp, A. Der-Avakian, L. R. Watkins, J. W. Rudy, and S. F. Maier, “Neonatal infection-induced memory impairment after lipopolysaccharide in adulthood is prevented via caspase-1 inhibition,” Journal of Neuroscience, vol. 25, no. 35, pp. 8000–8009, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. K. Morita, H. Sasaki, M. Furuse, and S. Tsukita, “Endothelial claudin: claudin-5/TMVCF constitutes tight junction strands in endothelial cells,” Journal of Cell Biology, vol. 147, no. 1, pp. 185–194, 1999. View at Publisher · View at Google Scholar · View at Scopus
  22. T. Nitta, M. Hata, S. Gotoh et al., “Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice,” Journal of Cell Biology, vol. 161, no. 3, pp. 653–660, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. C. J. Ek, M. D. Habgood, K. M. Dziegielewska, A. Potter, and N. R. Saunders, “Permeability and route of entry for lipid-insoluble molecules across brain barriers in developing Monodelphis domestica,” Journal of Physiology, vol. 536, no. 3, pp. 841–853, 2001. View at Publisher · View at Google Scholar · View at Scopus
  24. A. R. Wolff and D. K. Bilkey, “Immune activation during mid-gestation disrupts sensorimotor gating in rat offspring,” Behavioural Brain Research, vol. 190, no. 1, pp. 156–159, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. R. E. Fisher, N. A. Karrow, M. Quinton et al., “Endotoxin exposure during late pregnancy alters ovine offspring febrile and hypothalamic-pituitary-adrenal axis responsiveness later in life,” Stress, vol. 13, no. 4, pp. 334–342, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. S. L. Kjær, G. Wegener, R. Rosenberg, S. P. Lund, and K. S. Hougaard, “Prenatal and adult stress interplay—behavioral implications,” Brain Research, vol. 1320, pp. 106–113, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. D. Ibi, T. Nagai, Y. Kitahara et al., “Neonatal polyI:C treatment in mice results in schizophrenia-like behavioral and neurochemical abnormalities in adulthood,” Neuroscience Research, vol. 64, no. 3, pp. 297–305, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. N. Davies, A. Russell, P. Jones, and R. M. Murray, “Which characteristics of schizophrenia predate psychosis?” Journal of Psychiatric Research, vol. 32, no. 3-4, pp. 121–131, 1998. View at Publisher · View at Google Scholar · View at Scopus
  29. M. Weinstock, “Alterations induced by gestational stress in brain morphology and behaviour of the offspring,” Progress in Neurobiology, vol. 65, no. 5, pp. 427–451, 2001. View at Publisher · View at Google Scholar · View at Scopus
  30. G. Hava, L. Vered, M. Yael, H. Mordechai, and H. Mahoud, “Alterations in behavior in adult offspring mice following maternal inflammation during pregnancy,” Developmental Psychobiology, vol. 48, no. 2, pp. 162–168, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. S. J. Spencer, J. G. Heida, and Q. J. Pittman, “Early life immune challenge—effects on behavioural indices of adult rat fear and anxiety,” Behavioural Brain Research, vol. 164, no. 2, pp. 231–238, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. S. J. Spencer, S. Martin, A. Mouihate, and Q. J. Pittman, “Early-life immune challenge: defining a critical window for effects on adult responses to immune challenge,” Neuropsychopharmacology, vol. 31, no. 9, pp. 1910–1918, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. T. S. Reese and M. J. Karnovsky, “Fine structural localization of a blood-brain barrier to exogenous peroxidase,” Journal of Cell Biology, vol. 34, no. 1, pp. 207–217, 1967. View at Google Scholar · View at Scopus
  34. P. Lindahl, B. R. Johansson, P. Levéen, and C. Betsholtz, “Pericyte loss and microaneurysm formation in PDGF-B-deficient mice,” Science, vol. 277, no. 5323, pp. 242–245, 1997. View at Publisher · View at Google Scholar · View at Scopus
  35. C. J. Ek, K. M. Dziegielewska, H. Stolp, and N. R. Saunders, “Functional effectiveness of the blood-brain barrier to small water-soluble molecules in developing and adult opossum (Monodelphis domestica),” Journal of Comparative Neurology, vol. 496, no. 1, pp. 13–26, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. N. S. Harhaj and D. A. Antonetti, “Regulation of tight junctions and loss of barrier function in pathophysiology,” International Journal of Biochemistry and Cell Biology, vol. 36, no. 7, pp. 1206–1237, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. M. A. Petty and E. H. Lo, “Junctional complexes of the blood-brain barrier: permeability changes in neuroinflammation,” Progress in Neurobiology, vol. 68, no. 5, pp. 311–323, 2002. View at Publisher · View at Google Scholar · View at Scopus
  38. B. Engelhardt and L. Sorokin, “The blood-brain and the blood-cerebrospinal fluid barriers: function and dysfunction,” Seminars in Immunopathology, vol. 31, no. 4, pp. 497–511, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. Y. Sonobe, H. Takeuchi, K. Kataoka et al., “Interleukin-25 expressed by brain capillary endothelial cells maintains blood-brain barrier function in a protein kinase Cε-dependent manner,” Journal of Biological Chemistry, vol. 284, no. 46, pp. 31834–31842, 2009. View at Publisher · View at Google Scholar · View at Scopus